The Spirit of Fire was originally a colony ship, transporting colonists as well as equipment such as hydroponics and schools, in the UNSC's expansion efforts.[5]

Prior to the Battle of Arcadia, the Spirit of Fire had visited the planet Arcadia twice, once to aid in the colonization efforts taking place on the planet, and the second time to aid the local authorities in suppressing a violent student riot.[6]

More than fifty years after being constructed, it was recommissioned and refitted for military service prior to the period of history known as the Human-Covenant War. The last civilian captain of the Spirit of Fire was Captain Alexander, who had retired from active duty in the year 2520, on the 20th of July, after visiting the world of Verent. Directly after Alexander's retirement, the vessel was requisitioned by the UNSC and scheduled for refit in order to better prepare it for the combat operations in which it would participate.[7]

The ship was refitted with a Magnetic Accelerator Cannon and other armaments to serve as a warship. Huge storage bays that used to house machine parts now carry everything from M12 Warthogs and M808B Scorpions to construction supplies for fire bases involved in front line engagements or in rearguard actions and repair equipment for herself and other ships and crew. In 2530 the Spirit of Fire's thrust assemblies were replaced from the destroyer UNSC Calcutta, increasing output by 37%.[5]

After the events on Harvest, the Spirit of Fire arrived at the planet Arcadia, where it assisted in the evacuation of civilians, and the eradication of the Covenant from the planet's surface. When Professor Anders was captured by the ArbiterRipa 'Moramee, the Spirit of Fire quickly gave chase, following the Arbiter's flagship to an unknown planet in the Korinth Prior system.[9] This planet eventually turned out to be a ForerunnerShield World, containing a fleet of Forerunner warships. To ensure that the Covenant would not be able to use these warships against humanity, the reactor that powered the Spirit of Fire's Shaw-Fujikawa Translight Engine was detonated inside the Shield World's artificial sun by Sergeant John Forge. The ship managed to escape the exploding Forerunner installation, but without a functioning slipspace drive, the journey home would take many years, if not decades. Most of the crew entered cryonic sleep at this point, with only a skeleton crew remaining active to run the ship.[7]

On February 10, 2534,[10] the Spirit of Fire, previously designated as "missing", was declared "lost with all hands" by the UNSC. The reason for this change was kept top secret. A memorial service was held for the people aboard the vessel, but many of the crew's family members chose not to attend, holding out hope that their loved ones were still alive.[7] Various theories circulated throughout the UNSC as to the ship's actual fate, ranging from being lost during a covert mission for ONI, destroyed in orbit over Arcadia, defecting to Insurrectionist forces, or being stranded in space. When Mary Cutter, wife of CaptainJames Cutter, was asked about the defection theory, she physically assaulted the reporter.[11]

After the Human-Covenant War's conclusion, the Spirit of Fire was honored at the dedication of the living monument, along with numerous other ships that had been lost with all hands during the war.[12]

In March 2558 the freighter, Pilgrims Pride, was carrying several AC-220 Vultures and AV-22 Sparrowhawks that were previously attached to the Spirit of Fire.[13] The Pilgrims Pride launched a surprise attack on the UNSC Infinity and attempted to self-destruct inside the Infinity's bay. The Spartans managed to eject the freighter out of the bay. They also saved the Pilgrims Pride from total destruction by removing its exploding core. After recovering the remains of the attacking Vultures and Sparrowhawks, the crew used the ID numbers on the hulls to identify the ships as belonging to the Spirit of Fire. Confusing matters, the crew discovered that Pilgrims Pride had been constructed only five years earlier. While Commander Palmer speculated that the assault craft may have been stolen from the Spirit of Fire before the ship was lost, Roland pointed out that the assault craft were in fairly good condition for their age. Roland also determined that the freighter itself had been launched from Oth Lodon, a gas giant deep inside Jiralhanae-controlled space.[14]

Despite the diplomatic risks, Lord Hood, who felt guilty over his role in the Spirit of Fire's disappearance, ordered the Infinity to investigate. When they arrived at the coordinates, they found not the Spirit but ShipmasterVata 'Gajat's ship, which was docked to a massive glassing cannon. Captain Daniel Clayton contacted the Infinity, revealing himself to be aligned with the New Colonial Alliance. Intending to exact revenge on Lord Hood, Clayton fired three massive energy beams at the Infinity.[14] However, five SPARTAN-IVs managed to enter the station, stop Clayton and used the cannon to destroy 'Gajat's flagship.[15]

During the 27-year period, and despite the measures imposed by the Chief Medical Officer O'Neil, at least one Flood infection form managed to infiltrate the ship. In 2558, the Spirit of Fire had reached an unknown multiple star system and drifted near a terrestrial planet.[15]

Early concept art of Halo Wars suggests that a cat lived onboard the ship, possibly a pet to Captain Cutter. This is a possible reference to Jonesy, a cat that was lost aboard the UNSC Pillar of Autumn.

The Spirit of Fire has its own onboard news publication, The Spirit.[17]

^Halo Wars Timeline, 10 Feb 2534 (Unlockable after winning any game on repository), "The UNSC designates Spirit of Fire as "lost with all hands." The previous designation of "missing" had given hope to family and friends. The reason for the change is classified top secret. A memorial service is held for the crew, but many prominent family members do not attend, holding out hope that their loved ones are still alive."